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2-28-2001

Reproduction and food habits of the lined , Hippocampus erectus (Teleostei: ) of , Virginia.

R. L. Teixeira

John A. Musick Virginia Institute of Marine Science

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Recommended Citation Teixeira, R. L. and Musick, John A., Reproduction and food habits of the lined seahorse, Hippocampus erectus (Teleostei: Syngnathidae) of Chesapeake Bay, Virginia. (2001). Brazilian Journa of Biology, 61(1), 79-90. https://scholarworks.wm.edu/vimsarticles/2066

This Article is brought to you for free and open access by the Virginia Institute of Marine Science at W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. BIOLOGY OF THE LINED SEAHORSE 79

REPRODUCTION AND FOOD HABITS OF THE LINED SEAHORSE, Hippocampus erectus (TELEOSTEI: SYNGNATHIDAE) OF CHESAPEAKE BAY, VIRGINIA

TEIXEIRA, R. L.1 and MUSICK, J. A.2 1Museu de Biologia Prof. Mello Leitão, Av. José Ruschi, 4, CEP 29650-000, Santa Teresa, ES, 2Department of Fishery Science, School of Marine Science, The College of William and Mary, Gloucester Point, VA 23062, USA Correspondence to: Rogério L. Teixeira, Rua Bernardino Monteiro, 75, Centro, CEP 29650-000, Santa Tereza, ES, Brazil, e-mail: [email protected] Received August 26, 1999 – Accepted April 5, 2000 – Distributed February 28, 2001 (With 7 figures)

ABSTRACT The reproductive and feeding biology of the lined seahorse, Hippocampus erectus, was studied in Chesapeake Bay. are monogamous, and males incubate the eggs received from females in a closed brood pouch (= marsupium). Females do not play any parental care after mating. Total sex ratio and the operational sex ratio was strongly skewed toward females. Males and females had similar number of eggs/embryos and hydrated oocytes, respectively. The number of eggs/embryos found in the male brood pouch varied from 97 to 1,552 (fish from 80 to 126 mm TL), whereas the number of hydrated oocytes in female varied from 90 to 1,313 (fish from 60 to 123 mm TL). Both, the number of eggs/embryos and hydrated oocytes were better linearly correlated to total weight than to total length. The small snout and mouth size limits the feeding of the lined seahorse to small prey size. Amphypods were the predominant food items found in the guts, especially Ampithoe longimana, Gammarus mucronatus, and penantis. The lined seahorse is not abundant in Chesapeake Bay, but keeps a breeding population which is probably brought inside the bay by currents on drifting vegetation. Chances to find a partner may be difficult because of its low abundance, due to turbid waters, and its sedentary behavior. Key words: parental care, fecundity, fertility, amphipods, estuary.

RESUMO Reprodução e hábito alimentar do cavalo-marinho Hippocampus erectus (Teleostei: Syngnathidae) de Chesapeake Bay, Virgínia A biologia reprodutiva e alimentar do cavalo-marinho Hippocampus erectus foi estudada no estuário de Chesapeake Bay, Virgínia. Cavalos-marinhos são monógamos, sendo que o macho incuba os ovos recebidos da fêmea em uma bolsa incubadora fechada (= marsúpio). As fêmeas não desempenham qualquer cuidado com a prole após a fecundação. A razão sexual total e operacional foi fortemente direcionada para as fêmeas. Machos e fêmeas tiveram similares números de ovos/embriões e ovócitos hidratados, respectivamente. O número de ovos/embriões na bolsa incubadora dos machos variou de 97 a 1.552 (exemplares de 80 a 126 mm CT), enquanto o número de ovócitos hidratados nas fêmeas variou de 90 a 1.313 (exemplares de 60 a 123 mm CT). Tanto para os machos quanto para as fêmeas o número de ovos/embriões e ovócitos hidratados foi mais correlacionado com o peso do que com o comprimento total. O comprimento do focinho e a amplitude bucal limitam o cavalo-marinho a explorar pequenas presas. Anfípodas predominaram na dieta, especialmente Ampithoe longimana, Gammarus mucronatus e Caprella penantis. O cavalo-marinho não é uma espécie abundante em Che-

Rev. Brasil. Biol., 61(1): 79-90 80 TEIXEIRA, R. L. and MUSICK, J. A.

sapeake Bay, mas mantém uma população reprodutiva. As chances para encontrar um parceiro são pequenas, devido à baixa abundância, às águas túrbidas e ao comportamento sedentário da espécie. Palavras-chave: cuidado paternal, fecundidade, fertilidade, anfípodas, estuário.

INTRODUCTION small . Böhlke (1982) cited that the usual number of eggs in the brood pouch varies The lined seahorse, Hippocampus erectus from 250-400, and copepods, amphipods, and other Perry 1810, occurs from Nova Scotia to Uruguay, small crustaceans represented the principal prey being most common in deeper water where vege- for this seahorse. James & Heck (1994) observed tation is abundant, and can tolerate a marked range that variation in structural complexity in salinity and temperature (Böhlke, 1982). Male appears to have little effect on the foraging of the seahorses have sex role reversal. Fertilization and “sit and wait” visual predator lined seahorse, incubation of oocytes received from female takes whereas variation in light level produces significant place in a sac-like brood pouch (= marsupium) shifts in capture rates. located under the tail. After oocytes transference, This study attempts to assess the abundance, females do not play any role in parental care. Male and reproduction and food habits of the lined brood pouches in seahorses are the most advanced seahorse in Chesapeake Bay, with particular focus among all syngnathid , opening only through on the lower York River estuary. an anteromesial pore. Vincent et al. (1992) contested the fact that MATERIAL AND METHODS the seahorse, Hippocampus fuscus, is sex role reversed. These authors pointed out that the males The lined seahorse was collected with several of this seahorse are the predominant competitor fishing gears and in many different localities in for access to mates: males exhibit higher levels the lower Chesapeake Bay, Virginia. Most of them of behavior patterns, and males have the two most were collected in the lower York River, at stations, overtly aggressive behaviors in courtship, such as which support extensive beds of submerged aquatic tail wrestling and snapping with the snout. The vegetation (Fig. 1). The dominant eelgrass is point of view presented by Vincent et al. (1992), Zostera marina, which undergoes seasonal and that sex role reversal is not synonymous of parental annual fluctuations in distribution and abundance, care in syngnathids, creates confusion about unders- showing higher biomass during the spring and tanding sex role reversal. We will follow the tra- summer, and almost disappearing during the winter ditional and simplest idea that male syngnathids (Orth & Moore, 1984). have a brood pouch, which protect, osmoregulate For the biological analysis, samples were and aerate the eggs in compartments located in a taken from May through September 1992 primarily “placenta” (Linton & Soloff, 1964), which should with a 3 mm mesh dip net during low slack water be a female prerogative. Consistent to this idea, between Sarah’s’ Creek and the Coleman bridge Masonjones & Lewis (1966) observed that the (Station A), at approximately 37o24’N, 75o58’W dwarf seahorses, Hippocampus zosterae, are not (Fig. 1). Samples were taken at depth shallower courtship-role reversed, as previously assumed. than 1 m. Periodicity of dip net samples varied from There is little information on the biology of month to month. Additional samples were taken the lined seahorse. Fish (1952) reported underwater with: 1) A 10 m semi-balloon otter trawl. Each sound production for this seahorse. Linton & Soloff tow had a duration of five minutes at a speed of (1964) developed a physiological study of the male approximately 2.5 knots. The trawl survey program brood pouch. They found that the pouch provides consists on a monthly (excepting February) random optimum ionic and osmotic conditions for eggs/ stratified design survey of the lower Chesapeake embryos development. Hildebrand & Schroeder Bay, and fixed station mid-channel transects in each (1928) cited that H. hudsonius (= H. erectus) is of the three major Virginia tributaries: the York, not very common in Chesapeake Bay, it can reach James, and Rappahannock rivers (Bonzek et al., 150 mm, and its food habits appears to consist of 1993).

Rev. Brasil. Biol., 61(1): 79-90 BIOLOGY OF THE LINED SEAHORSE 81

77º00' 76º00'

Rappahannock

38º00'

Richmond York

Atlantic Ocean

A James B

37º00' 010203040

Nautical miles Norfolk

Fig. 1 — Map of the study area in Chesapeake Bay from May 1992 through August 1994 by the trawl survey program (o), and in the lower York River with dip net (Station A) and crab scrape (Station B).

Trawl survey samples were taken from May pendicular to the longitudinal axis of the tail (Böhlke, 1992 through August 1994, and for the biological 1982); total body and gonad weights (0.001 g) were analysis, only the fish saved by the trawl survey also recorded. Ovary weight (0.001 g) was recorded staff were used; 2) A crab scrape apparatus, 0.5 to calculate the gonadosomatic index (GSI = ovary × 1.5 m with 5 mm mesh size, was used from June weight/total weight × 100). through August 1993 (Station B), and was spo- The number of eggs or embryos in the male’s radically used in other months. brood pouch and the number of pre hydrated oocy- Trawl survey data from January 1988 through tes in the ovaries were counted for fecundity and December 1993 was used to observe abundance, fertility comparisons between males and females. and the relationship to salinity and temperature. The following scale was used to separate different Between years, abundance was compared by one- eggs/embryos stages: 0 – non pregnant males; 1 – way analyses of variance (ANOVA). eggs newly deposited in the pouch; 2 – embryos Fish were preserved in 10% formalin for a in the beginning stage of development or still con- maximum of 24 h, and then washed and transferred taining yolk sac; and 3 – embryos without yolk to 70% ethanol. Laboratory procedures included: sac, ready to be released. Analysis of covariance identification of species based on Böhlke (1982); (ANCOVA) was employed to test slopes between measurement of each specimen for total length (TL cases. Data analyses were performed on log trans- in mm), from the top of head to the tip of tail where formed data due to inequality of variances. Log the tail is straightened and the head oriented per- transformations were employed after testing for

Rev. Brasil. Biol., 61(1): 79-90 82 TEIXEIRA, R. L. and MUSICK, J. A.

homogeneity of variances using the Bartlett’s test 1993. No significant differences were found in

(SAS Institute, 1985). abundance among years (ANOVA: F1,278 = 1.15; Only the first portion of the guts was used P > 0.34) (Fig. 2A). Pooled monthly data showed for assessing the diet of the lined seahorse. Prey that abundance increased from April to June, and were identified to the lowest taxon wherever pos- from September to November (Fig. 2B), while only sible, and quantified by frequency of occurrence a few specimens were collected during the winter (%F.O.) and number (%N). For assessing possible months. The second peak in abundance from variation in the diet, specimens were divided in September to November seems to be related to the three length groups: 1) small (<60 mm TL); 2) mid recruitment of juveniles. Lined seahorse occurred sized (60-99 mm TL); and 3) large (>99 mm TL). in temperatures that ranged from 5.0 to 28oC, and in salinities from 9.2 to 35.5‰. There was no RESULTS correlation between abundance and these abiotic parameters. A total of 136 seahorses ranging in The trawl survey program collected 448 lined size from 23 to 126 mm TL were examined for seahorses from January 1988 through December biological data during the study.

120 A 100 98 91 84 80

61 60 60 54

40 Number of specimens

20

0 1988 1989 1990 1991 1992 1993

100 B 84 84 80

63 60

46 43 40 39 40 Number of specimens

20 17 16 7 9 No samples 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 2 — Abundance of the lined seahorse in Chesapeake Bay. A) Inter-annual variation in abundance of fish sampled with otter-trawl from January 1988 through December 1993. B) Pooled monthly abundance of fish sampled with otter-trawl from January 1988 through December 1993.

Rev. Brasil. Biol., 61(1): 79-90 BIOLOGY OF THE LINED SEAHORSE 83

Total sex ratio was skewed toward females. be released. Total length of males and females were From the fish examined, 40 were males, 66 females, similar (Fig. 3). The gonadosomatic index of females and the remained immatures. Total male-female sex larger than 70 mm TL varied from 0.26% to 13.44%. ratio was 0.6:1, which was significantly different Based on pooled data, mean gonadosomatic index from the expected 1:1 ratio (χ2 = 60.37; P > 0.05). varied from 0.51% in April to 7.33% in August (Fig. Sixteen males were pregnant, whereas 38 females 4). The reproductive period of the lined seahorse had running-ripe ovaries. No one of the examined in Chesapeake Bay appeared to start in May and females had ovaries with hydrated oocytes, read to finished in October.

30 Female Male 25 Immature

20

15

10 Number of specimens

5

0 20 30 40 50 60 70 80 90 100 110 120 Total length (mm)

Fig. 3 — Total length frequency distribution of the lined seahorse used to assess the reproductive and feeding biology, collected with different fishing gears from May 1992 through September 1993.

14

6 12 5 7 10 21

8

GSI 14 6

4

2 3 2 1 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 4 — Gonadosomatic index (GSI) of females of the lined seahorse of Chesapeake Bay. Bars = mean GSI; vertical lines = standard deviation.

Rev. Brasil. Biol., 61(1): 79-90 84 TEIXEIRA, R. L. and MUSICK, J. A.

Males and females showed similar numbers The number of eggs/embryos (E) or pre-hy- of eggs or embryos and pre-hydrated oocytes, drated oocytes (O) was better correlated with total respectively, and number of eggs/embryos and weight (TW) than total length (TL). The regression oocytes were correlated with size and weight (Fig. equations were: 5A and B). ANCOVA showed that there was no significant difference between number of eggs and E = 10.22 TL – 604.76 (n = 16; r2 = 0.45; P < 0.02); number of pre-hydrated oocytes using length as E = 67.43 TW + 16.14 (n = 16; r2 = 0.57; P < 0.01); 2 the covariate (F1.38 = 0.36; P > 0.55). The number O = 15.18 TL – 865.55 (n = 38; r = 0.59; P < 0.01); of eggs/embryos counted inside the brood pouch O = 138.87 TW – 30.44 (n = 38; r2 = 0.73; P < 0.01). ranged from 97 to 1,552 (mean = 451; SD = 232.1), in males which varied in total length from 80 to Non fertilized eggs frequently occurred inside 126 mm. The number of pre-hydrated oocytes in the male brood pouch. They were observed in females varied from 90 to 1,313 (mean = 460; SD = 50.0% of the analyzed males, and they represented 253.3), where total length ranged from 60 to 123 from 1.72% to 32.9% of the total number of eggs/ mm. embryos in the brood pouch.

1,400 Male 1,200 Female Linear (male) 1,000 Linear (female)

800

600

400 Number of eggs/embryos 200 A 0 50 60 70 80 90 100 110 120 130

Total length (mm)

1,600 Male 1,400 Female 1,200 Linear (male) Linear (female) 1,000 800 600 400 200 Number of eggs/embryos B 0 024681012

Total weight (g)

Fig. 5 — Relationship between fecundity and fertility of the lined seahorse of Chesapeake Bay. A) Relationship between number of eggs/embryos or oocytes against total length. B) Relationship between number of eggs/embryos or oocytes against total weight.

Rev. Brasil. Biol., 61(1): 79-90 BIOLOGY OF THE LINED SEAHORSE 85

Fertilized eggs in the pouch are irregular but that during the winter (temperature of 10.6oC) in spherical in shape, while pre-hydrated oocytes are the Mid-Atlantic Bight, the lined seahorse was cuneiform. Hydrated oocytes may have a shape found motionless on the bottom, with its prehensile similar to that of eggs newly deposited in the male tail straightened, and exhibited no noticeable pouch. The pre-hydrated oocytes all had similar respiratory movement. diameter, evidence that the lined seahorse is a total Abundance of the lined seahorse inside Che- spawner. sapeake Bay did not vary significantly from 1988 From the fish collected, 133 (97.8%) had full through 1993. The results were based on trawl guts. Feeding of the lined seahorse is limited by survey stations, which do not sample the main snout shape and width, as is the case with other eelgrass beds inside the bay. Sampling of eelgrass syngnathids. Amphipods were the most important beds in the lower Chesapeake Bay by Orth & Heck prey, followed by copepods. The most important (1980), showed that the seahorses were not abun- identified amphipods for frequency of occurrence dant there, and represented only 0.02% of all fish and by numerical abundance in the gut were: Ampi- collected. Ichthyoplankton samples taken in eel- thoe longimana, Gammarus mucronatus, Caprella grass beds in the lower Chesapeake Bay by Olney penantis and Stenothoe minuta (Table 1). & Boehlert (1988), did not find the presence of Ampithoe longimana was more frequently any newborn seahorses, only larger juveniles and found, whereas G. mucronatus was the most prey these were low in abundance. Based on the fertility found. Besides some small crustaceans, other of this seahorse, it is noted that just a single male groups, such as mollusks and polychaetes, did not could release more newborn than the entire number represent important items in the diet of the lined of seahorses collected by the trawl survey program seahorse. during the six years. Length groups analyzed frequency of prey Number of specimens of the lined seahorse in the guts, and amphipods were most frequent in inside Chesapeake Bay could also be related to all size groups (Figs. 6 and 7). Smaller fish the abundance of seagrass and drifting vegetation, (<60 mm TL) fed mainly on amphipods, with once the syngnathids become dependent on it. Orth copepods secondarily important. Mid size (60- & Moore (1984) pointed out that eelgrass has 99 mm TL) and larger (>99 mm TL) fed almost suffered several historical fluctuations in abun- exclusively on amphipods. Ampithoe longimana dance, and the causes of this decline may be related was most frequent in the smaller and larger fish to changes in water quality, primarily increased gut contents, and G. mucronatus was most frequent eutrophication and turbidity, and diseases. in the mid size group. The number of pre-hydrated oocytes pro- duced by the female lined seahorse is similar to DISCUSSION the number of eggs/embryos found in the male brood pouch. Relatively few specimens of the lined This suggests that similar sized partners seahorse occupy Chesapeake Bay. As a weak-swim- should mate, in order to maximize the total number ming fish, probably some individuals are acci- of oocytes present in the female ovary, since the dentally brought inside the bay by ocean currents, lined seahorse is a total spawner and is mono- when they are attached to drifting vegetation. Des- gamous. However, as hydrated oocytes are very pite the lined seahorse can tolerate a wide range ephemeral, and partners with different size could of salinity (Böhlke, 1982; this study), the Chesa- mate, many oocytes may not be transferred to the peake Bay appears not to be very conducive for male brood pouch in the case of a larger female this seahorse, even though the estuary furnishes than male, because the number of young is also an excellent habitat for shelter and feeding, and dependent on male brood pouch carrying capacity. this species can breed inside an estuarine habitat. On the other hand, if the male is larger than the Migratory movements have not been recorded for female, a female will not have enough hydrated this seahorse, but they are even more rare in Che- oocytes to fill the male brood pouch. Both cases sapeake Bay during the winter, especially at the represent a trade off between timing to mate and lower York River. Wicklund et al. (1966), observed maximization of spawn.

Rev. Brasil. Biol., 61(1): 79-90 86 TEIXEIRA, R. L. and MUSICK, J. A.

TABLE 1 Food items found in the guts of the lined seahorse, Hippocampus erectus, of Chesapeake Bay. %F.O. = frequency of occurrency; %N = number of prey.

Prey %F.O. %N CRUSTACEA Copepoda 11.4 8.4 Ostracoda 0.9 <0.1 Amphipoda Ampithoidae Ampithoe longimana 35.1 13.6 Cymadusa compta 5.3 0.7 Corophiidae Cerapus tubularis 1.7 0.4 Corophium tuberculatum 5.3 0.7 Ischyroceridae Jassa falcata 5.3 1.6 Bateidae Batea catharinensis 0.9 <0.1 Gammaridae Elasmopus levis 2.6 0.4 Gammarus mucronatus 33.3 39.8 Melita appendiculata 4.4 0.7 Pleustidae Sympleustes glaber 0.9 <0.1 Stenothoidae Stenothoe minuta 21.9 7.4 Ampeliscidae Ampelisca vadorum 0.9 <0.1 Ampelisca verrilli 1.7 0.3 Aoridae Rudilemboides sp. 0.9 0.2 Caprella penantis 22.8 12.6 Other Caprellids 13.2 2.1 Unidentified Amphipods 21.9 8.5 Amphipod Remains 4.4 Isopoda Idotheidae Erichsonella attenuata 0.9 0.2 Mysidacea Mysidopsis bigelowi 0.9 <0.1 Decapoda

Rev. Brasil. Biol., 61(1): 79-90 BIOLOGY OF THE LINED SEAHORSE 87

TABLE 1 (Continuation)

Prey %F.O. %N Palaemonidae pugio 2.6 0.4 Palaemonetes vulgaris 1.7 0.3 Crangonidae Crangon septemspinosa 3.5 0.4 Portunidae Callinectes sapidus (megalopa) 3.5 0.6 Gastropoda Cerithiidae Bittium varium 0.9 <0.1 POLYCHAETA 2.6 0.3 MISCELANEOUS 0.9

This seems to be true, since the search for (1992) usually found from 250 to 400 eggs, while a mate in the eelgrass beds could take a long time, pointing out that the results reported by Lockwood causing atresia in the hydrated oocytes. The weak (1867) was not confirmed again. relationship obtained between fecundity and fertility In this study, it was observed that a large (Fig. 2), provides evidence that a male may not female could carry up to 1,000 oocytes, whereas always have a full brood pouch. the largest number of eggs/embryos inside the Gravid females outnumbered available males male’s brood pouch obtained during this study was (with total developed brood pouch) by up to two 1,552. The amount of oocytes that can be trans- times. This means that the males are the limiting ferred to the male brood pouch depends on the sex for reproductive success inside Chesapeake male’s carrying capacity. The largest specimen Bay. Since seahorses are monogamous (Vincent recorded by Böhlke (1992) was 173 mm TL, much et al., 1992), most females will not find a mate longer than that observed in this study: 126 mm TL. during the reproductive period. The investment Fecundity and fertility in the largest specimens in ovary development for this particular lined sea- during this study was found to exceed 1,000 eggs. horse “population” which occupies Chesapeake The limitation of prey in many syn- Bay is therefore a trade-off between the chance gnathid species has been attributed to snout size of finding a mate and waste of energy. In fact, there (and width) by many authors (e.g., Mercer, 1973; is no record in the literature that the ovaries can Brook, 1977; Teixeira & Musick, 1995). In Chesa- be recovered after the first mating, or whether peake Bay, the food habits of the lined seahorse males could receive another batch after releasing mostly resemble that of the northern, Syngnathus embryos from the pouch. Newborn seahorses are fuscus, and the dusky pipefish S. floridae (Mercer, released by ejection from the brood pouch by body 1973; Teixeira & Musick, 1995). Amphipods were contortions and a pumping action of the pouch. the most important prey for all length groups ana- The period of pregnancy may represent a high lyzed, but copepods are probably more important energetic cost for the male seahorse, which may for the newborn seahorse. reach extremes during the time they are giving birth. Acknowledgments — This paper was funded by Conselho Fertility in the lined seahorse may vary in Nacional do Desenvolvimento Científico e Tecnológico (Process N. 302657/87-8). We appreciate Thomas A. Munroe, different habitats. Lockwood (1867) reported up Romuald N. Lipcius, Robert J. Orth, and Wolfgang Vogelbein to 1,000 juveniles inside the brood pouch. Böhlke for useful criticisms of an earlier version of the manuscript.

Rev. Brasil. Biol., 61(1): 79-90 88 TEIXEIRA, R. L. and MUSICK, J. A.

Amphipods 76.9% <60 mm (n = 26)

Palaemonids 3.8% Polychaetes 3.8%

Copepods 36.4%

60-99 mm (n = 67) Amphipods 95.5%

Palaemonids 1.5% Polychaetes 1.5% Copepods 4.5%

>99 mm (n = 21) Amphipods 95.2%

Gastropods 4.8%

Palaemonids 9.5% Polychaetes 4.8%

Fig. 6 — Food items most frequently found in the guts of the lined seahorse of Chesapeake Bay.

Rev. Brasil. Biol., 61(1): 79-90 BIOLOGY OF THE LINED SEAHORSE 89

Ampithoe longimana 34.6% <60 mm (n = 26)

Caprella penantis 7.7%

Stenothoe minuta 15.4% Gammarus mucronatus 15.4%

60-99 mm (n = 67)

Caprella penantis Ampithoe longimana 26.9% 34.3%

Stenothoe minuta 23.9% Gammarus mucronatus 44.8%

Ampithoe longimana 52.4% >99 mm (n = 21)

Caprella penantis 33.3% Stenothoe minuta 23.8%

Gammarus mucronatus 23.8%

Fig. 7 — Amphipod species identified the guts of the lined seahorse of Chesapeake Bay.

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